APHIDICIDAL AND DETERRENT ACTIVITY OF PHENOLIC ACID EXTRACTS FROM SOME HERBAL PLANTS TOWARDS MYZUS PERSICAE SULZ. AND RHOPALOSIPHUM PADI L.

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1 APHIDICIDAL AND DETERRENT ACTIVITY OF PHENOLIC ACID EXTRACTS FROM SOME HERBAL PLANTS TOWARDS MYZUS PERSICAE SULZ. AND RHOPALOSIPHUM PADI L. Pawel Czerniewicz *, Grzegorz Chrzanowski, Hubert Sytykiewicz, Iwona Sprawka, Bogumil Leszczynski Department of Biochemistry and Molecular Biology, Siedlce University of Natural Sciences and Humanities, Prusa 12, Siedlce, Poland ABSTRACT The naturally-occurring phenolic acid mixtures from selected herbal plants were tested for their deterrent and aphidicidal activity towards two aphid species, the peach-potato aphid, Myzus persicae (Sulz.) and the bird cherry-oat aphid, Rhopalosiphum padi (L.). The phenolic acids were extracted from Hypericum perforatum (L.), Juglans regia (L.), Mentha piperita (L.) and Sambucus nigra (L.). The obtained results indicated that the phenolic acid extracts negatively affected the development of both aphid species. Their influence was demonstrated by prolongation of the prereproductive period, a reduction in daily fecundity and a decrease in the intrinsic rate of natural increase. Among the tested plants, extracts from J. regia and M. piperita showed the most promising results. The phenolic acids obtained from these plants, not only significantly reduced the number of aphids on host plant, but also limited initial infestation in choiceleaf bioassays. Furthermore, the oligophagous bird cherry-oat aphid was more sensitive to the applied concentrations of the phenolic extracts than the highly polyphagous peach-potato aphid. It is concluded that phenolic acids naturally occurring in the donor plants might be used as biopesticides in aphid control. KEYWORDS: botanical insecticides, phenolic acid extracts, peach-potato aphid, bird cherry-oat aphid, feeding deterrents. INTRODUCTION Aphids are considered one of the most important insect pests. Because of its capacity for extremely rapid reproduction, they can develop high population density in relatively short period of time. Aphids cause serious damage to the plants, both by direct feeding and by the transmission of plantpathogenic viruses. While feeding, aphids ingest phloem sap and secrete within saliva toxic compounds, that disturb growth and development of infested plants [1, 2]. The peach-potato aphid (Myzus persicae Sulz.) has an extremely wide host range of over 40 different plant families including a wide variety of vegetable and ornamental crops. On the other hand, the bird cherry-oat aphid (Rhopalosiphum padi L.) belongs to oligophagous species that cause significant crop losses in cereals [3]. Aphid populations are usually controlled with the use of insecticides [4]. However, frequent applications of synthetic pesticides have different drawbacks, such as increasing pest resistance, residues in food, and deleterious impact on environment. There are also problems of negative effects on non-target organisms, including humans [5, 6]. Therefore, in recent years the research on alternative methods of aphid control has become more important. One of the alternative strategy to chemical insecticides is the use of plant-derived extracts, which are often more selective, biodegradable, and generally have little or no harmful effects on non-target organisms. Furthermore, thanks to the fact that botanical insecticides contain mixtures of biologically active substances, the chances of developing pest resistance are less likely [7, 8]. The insecticidal properties of Juglans regia L. extracts against different kind of pests have been reported by numerous research papers [9-12]. Active compounds extracted from Mentha piperita L. acted as a repellent to Brevicoryne brassicae L. [13] and were toxic to Tetranychus cinnabarinus Boisd. [14]. There are also several data on the insecticidal properties of extracts from Hypericum perforatum L. [15] and Sambucus nigra L. [16, 17]. Plants have long been considered as a rich source of biologically active metabolites. One of the most active chemicals produced by plants are phenolic compounds including phenolic acids. These substances are well known from their antioxidant, anticancer and antimicrobial activities [18, 19]. Moreover, many of these phytochemicals play an important role in defence mechanisms and can be used as anti-herbivore agents in plant 5714

2 protection. Earlier studies demonstrated that different groups of phenolics may discourage insect herbivory, either by deterring feeding and oviposition or by impairing settling and larval growth [20, 21]. In laboratory bioassays, it was shown that phenolic acids extracted from J. regia strongly limited fecundity and development of the grain aphid (Sitobion avenae L.) [12]. The present paper reports on the effect of phenolic acid extracts obtained from H. perforatum, J. regia, M. piperita and S. nigra on settling behavior as well as on growth and development of two aphid species, the highly polyphagous peach-potato aphid and the oligophagous bird cherry-oat aphid. MATERIALS AND METHODS Insect cultures. The aphids used in this study came from a stock culture kept at the Siedlce University of Natural Sciences and Humanities, Poland. Parthenogenetic clone of M. persicae was reared on pea seedlings (Pisum sativum L. cv. Szesciotygodniowy) whereas R. padi was reared on winter wheat (Triticum aestivum L. cv. Tonacja). Insect cultures were maintained in a climatic chambers at 22 C, 16:8 LD photoperiod, and 70% RH. The adult apterous females were selected for all subsequent experiments. TABLE 1 Plant species used for preparing phenolic acid extracts. Scientific name Family Plant part used Hypericum perforatum L. Hypericaceae Leaves and flowers Juglans regia L. Juglandaceae Leaves Mentha piperita L. Lamiaceae Leaves and flowers Sambucus nigra L. Caprifoliaceae Leaves Phenolic acid extracts. Phenolic acid mixtures were obtained from four medicinal plants (Table 1). The herb of H. perforatum and M. piperita were got from herbal shop, while the leaves of J. regia and S. nigra were collected from small private orchard located in Siedlce. The procedure of phenolic acid extraction was based on the method described by Kowalski and Wolski [22]. Extraction of the phenolic acids was performed using 50 g of dry crushed plant material with 80% methanol. Pigments and fatty substances were removed with petroleum ether and the extracts were then cleared with sodium hydrogen carbonate (5% final concentration). The mixtures were acidified to ph 2.0 with 6 M hydrochloric acid and the phenolic acid fraction was immediately extracted with ethyl acetate. The organic phase was evaporated to dryness under a vacuum at 40 C. Residues of phenolic acids were weighed and then dissolved in 20 ml of 80% ethanol (stock solution). Spraying mixtures were prepared from the stock solution after further dissolving with distilled water containing 0.05% Tween 80 and 4% ethanol. Estimation of deterrent activity. The deterrent effect of three concentrations of phenolic acid extracts (0.05%, 0.1% and 0.2%) towards M. persicae and R. padi were tested. The aphids were offered a choice between extract-treated and control leaves. Leaves cut from suitable host plant (pea or wheat) were dipped for 10 s in the extracts or control solution (water containing 0.05% Tween 80 and 4% ethanol) and dried at room temperature. Afterwards, treated and control leaves were transferred into Petri dishes (20 cm diameter) lined with moistened filter paper. A group of 20 aphids (1-hour starved) were placed between the leaves at the centre of the dish, and after 24 h the number of insects present on each leaf were recorded. The deterrence index (DI) was calculated for each extract using the formula according to Pascual and Robledo [23]: DI = [(C-T)/(C+T)] x 100%, C the number of aphids on control leaves; T the number of aphids on treated leaves. Estimation of aphidicidal activity. Two concentrations of phenolic acids (0.05% and 0.2%) from each plant were used to determine the influence of the plant extracts on M. persicae and R. padi development. The experiment took place in a climatic chamber at 22 C, 16:8 LD photoperiod, and 70% RH. Seven-day old pea and winter wheat seedlings were infested with a wingless adult females of M. persicae or R. padi, respectively. A single aphid was then isolated with a Plexiglas tube with cooling fans for ventilation. When females started to produce offsprings, five nymphs were left on each seedling and the other offsprings and the adult were removed. The young nymphs (two-day old) were sprayed with the tested phenolic acid mixtures or 0.05% Tween in 4% ethanol (control) using 0.2 ml of the solution per plant. The treatment was repeated twice at 5-days intervals (when the aphids reached maturity, and then, during their reproductive activity). The following parameters were measured: i) larval developmental time (prereproductive period, PRP), ii) daily fecundity of females (DF) and iii) number of aphids on plant at the end of experiment. These data were used to determine the influence of the plant extracts on M. persicae and R. padi population development. The intrinsic rate of natural increase (r m) was calculated according to Wyatt and White [24]. r m = x (ln Md) x d -1, where: d is the length of the prereproductive period; Md is the number of larvae produced in a reproductive period equal to d and is the correction factor. 5715

3 Biological efficacy of phenolic acid extracts for the aphids was expressed using Abbott's correction [25]. Statistical analysis. The analyses for determination of deterrent activity of extracts containing phenolic acids from tested plants against R. padi and/or M. persicae as well as the effect of these extracts on the growth and development of the insects were carried out in ten independent replicates. Differences between number of aphids on seedlings sprayed with the extracts and number of the insects on control (non-treated) seedlings were calculated using Student s t-test. Kruskal-Wallis test (nonparametric equivalent of ANOVA) was calculated for evaluation of the diversity in the parameters of aphids development (prereproductive period, PRP; daily fecundity, DF; intrinsic rate of natural increase, r m and number of insects on the end of the experiment) under treatment with extracts. Significance of differences between mean values was calculated using Tukey s post-hoc test at P < All calculations were carried out using Statistica 10.0 software (Statsoft, Poland). RESULTS The choice-leaf bioassay showed that M. persicae and R. padi generally avoided leaves treated with phenolic acid mixtures and the observed effect intensified with increasing phenolics concentration. Among plant extracts, the most active were phenolic acids obtained from J. regia and M. piperita (Table 2, Table 3). All tested concentrations of phenolic acids from J. regia significantly deterred peachpotato aphid and bird cherry-oat aphid, for which the deterrence index ranged from 17.7% to 41.3% and 10.1% to 34.8%, respectively. Whereas extracts from M. piperita showed deterrent properties at the concentration of 0.1% and 0.2% with values of deterrence index for M. persicae between 28.8% and 36.2%, and for R. padi between 21.3% and 42.5%. In the case of extracts from H. perforatum and S. nigra, both aphid species avoided treated leaves only after application the highest concentration of phenolic acid mixtures. However, as indicated values of deterrence index, the aphid response was weaker than that observed for extracts from J. regia and M. piperita. The tested phenolic acid extracts affected the development of peach-potato aphid and the observed effect was dose-dependent (Table 4). The PRP values of M. persicae were prolonged by about 0.5 TABLE 2 Deterrent activity of phenolic acid extracts towards peach-potato aphid. Phenolic acid extracts Conc. (%) Mean number of females ± SD Test Control H. perforatum ± ± ± ± ± ± J. regia ± ± ± ± 1.6 < ± ± 2.0 < M. piperita ± ± ± ± ± ± 3.1 < S. nigra ± ± ± ± ± ± 2.0 < P confidence level of differences from the control (Student s t-test). TABLE 3 Deterrent activity of phenolic acid extracts towards bird cherry-oat aphid. Phenolic acid extracts Conc. (%) Mean number of females ± SD Test Control H. perforatum ± ± ± ± ± ± J. regia ± ± ± ± 1.9 < ± ± 2.6 < M. piperita ± ± ± ± ± ± 3.0 < S. nigra ± ± ± ± ± ± P confidence level of differences from the control (Student s t-test). P P Deterrence index DI% Deterrence index DI% 5716

4 day after application of 0.2% phenolic acid mixtures from J. regia and S. nigra. Moreover, all plant extracts at a higher concentration caused a significant decrease in production of larvae by apterous females. The most active were phenolic acids from J. regia and M. piperita that limited daily fecundity by about 1.6 offspring comparing to the control. The peach-potato aphid submitted to a higher concentration of phenolic acids also showed significant reduction in values of the intrinsic rate of natural increase, and similarly the strongest reduction was observed after application of the extract from J. regia followed by extracts from M. piperita, S. nigra and H. perforatum. In tests concerning the bird cherry-oat aphid development, application of phenolic acid extracts from all tested plants at concentration 0.2% and phenolics from J. regia at concentration 0.05% significantly prolonged prereproductive period (Table 5). Among tested extracts, the most active were phenolic acids from J. regia and M. piperita, where values of PRP were prolonged by 1.9 and 1.1 day, respectively. It was also found that all phenolic acid mixtures, with the exception of H. perforatum at 0.05% concentration, significantly decreased daily fecundity of R. padi females. During the experiment, unsprayed aphids produced 5.2 larvae per day. Application of the phenolic acid extracts at concentration of 0.2% reduced daily fecundity of the females by offspring and the strongest effect occurred after treatment with extract from J. regia. Moreover, phenolic acids obtained from J. regia reduced the value of the intrinsic rate of natural increase much stronger, than those from M. piperita, S. nigra and H. perforatum. Treatments with phenolic acid extracts from tested plants caused a significant decrease in the number of M. persicae and R. padi individuals recorded at the end of the experiment (Table 6). Additionally, extracts contained higher concentrations of the phenolic acids caused an increase in efficacy towards studied aphids. The highest effectiveness of the tested mixtures against peach-potato aphid was shown after application of 0.2% phenolic acids from J. regia (approximately 74%), followed by 0.2% extracts from M. piperita, S. nigra and H. perforatum with efficacy of 70%, 53% and 49%, respectively. Generally, the tested phenolics showed stronger activity towards R. padi than M. persicae. Treatments of the bird cherry-oat aphid with all tested extracts at concentration 0.2% resulted in efficacy above 70%, and in the case of the extracts from J. regia and M. piperita the efficacy even reached 80.6% and 88.54%, respectively. TABLE 4 Effect of phenolic acid mixtures extracted from tested plants on population parameters of M. persicae. Treatment Conc. (%) PRP DF rm H. perforatum ± 0.34 ab 2.27 ± 0.73 a 0.28 ± 0.04 a ± 0.42 ab 1.33 ± 0.50 bc 0.22 ± 0.03 bc J. regia ± 0.27 ab 1.84 ± 0.64 ab 0.26 ± 0.04 ab ± 0.30 a 0.86 ± 0.47 c 0.17 ± 0.05 c M. piperita ± 0.48 ab 1.83 ± 0.65 ab 0.26 ± 0.04 ab ± 0.31 ab 0.97 ± 0.54 c 0.19 ± 0.05 c S. nigra ± 0.32 ab 2.04 ± 0.65 ab 0.26 ± 0.04 ab ± 0.27 a 1.38 ± 0.62 bc 0.21 ± 0.06 bc Control 7.15 ± 0.40 b 2.54 ± 0.46 a 0.30 ± 0.02 a H (8, 90) P < < PRP prereproductive period (days); DF daily fecundity per female; r m intrinsic rate of natural increase. Means (± SD) within columns followed by the same letter are not significantly different at the P 0.05 (Tukey s test). TABLE 5 Effect of phenolic acid mixtures extracted from tested plants on population parameters of R. padi. Treatment Conc. (%) PRP DF rm H. perforatum ± 0.46 cd 4.46 ± 1.06 ab 0.42 ± 0.04 ab ± 0.29 bc 2.40 ± 1.02 cd 0.32 ± 0.06 d J. regia ± 0.73 bc 2.64 ± 1.07 cd 0.33 ± 0.05 cd ± 0.52 a 1.02 ± 0.50 e 0.19 ± 0.05 e M. piperita ± 0.22 cd 3.35 ± 0.94 bc 0.39 ± 0.04 bc ± 0.44 b 1.70 ± 0.61 de 0.27 ± 0.06 d S. nigra ± 0.13 d 3.96 ± 0.95 b 0.42 ± 0.04 ab ± 0.42 bc 2.08 ± 0.73 de 0.30 ± 0.05 d Control 5.25 ± 0.25 d 5.23 ± 0.90 a 0.46 ± 0.03 a H (8, 90) P < < < PRP prereproductive period (days); DF daily fecundity per female; r m intrinsic rate of natural increase. Means (± SD) within columns followed by the same letter are not significantly different at the P 0.05 (Tukey s test). 5717

5 TABLE 6 Biological efficacy of phenolic acid extracts from tested plants against peach-potato aphid and bird cherry-oat aphid. Treatment Conc. (%) M. persicae R. padi Number of aphids a Efficacy (%) Number of aphids a Efficacy (%) H. perforatum ± 29.2 ab ± 24.7 b ± 18.7 cde ± 22.1 de J. regia ± 22.6 abcd ± 21.7 cd ± 9.3 e ± 7.9 e M. piperita ± 22.9 bcd ± 18.5 bc ± 12.4 e ± 11.3 de S. nigra ± 24.6 abc ± 21.0 b ± 20.9 de ± 12.1 de Control 83.9 ± 13.4 a ± 27.2 a - H (8, 90) P < < a number of aphids on plant (mean ± SD) at the end of the experiment. DISCUSSION Aphids accept plants as a hosts only when they use it as a source of food. Therefore, the number of aphids that settle and feed on a leaves treated with a given extracts is a good indicator of its suitability [26]. The current study demonstrated that application of phenolic acid extracts obtained from J. regia, M. piperita, S. nigra and H. perforatum inhibited peach-potato aphid and bird cherry-oat aphid settling on the treated leaves. Such effect can be related to biological activity of phenolic acids present in the extracts. Urbanska et al. [27], using the electrical penetration graph (EPG) technique, demonstrated that the grain aphid avoided feeding on diets containing phenolic acids, that manifested itself a strong reduction in probing activity, especially in case of gallic, caffeic and chlorogenic acids. The studied phenolic acid extracts showed different level of deterrent activity toward M. persicae and R. padi, depending on the plant species and applied concentrations. Among the studied extracts, the most active was the mixture of phenolic acids obtained from J. regia and M. piperita, since after their applications at the highest concentrations their deterrence index ranged between 34.8 and 42.5%. However, the observed deterrent effect should be considered as relatively weak, since several authors revealed much greater effectiveness of plant extracts in choice bioassays. Chermenskaya et al. [28], in tests towards Schizaphis graminum (Rond.), showed deterrent activity of ethanolic extracts of several Kyrgyzstan plants greater than 80%. According to Castillo et al. [29], a good anti-settling activity in tests concerning aphids is achieved only when settling inhibition effect on treated leaves is higher than 70%. Relatively low deterrent activity of some extracts in the present experiment may be explained by complex aphids behavior during host-plant selection that involve several chemical and physical cues. Thus, the stimuli causing rejection of the plant by aphids may become relevant at a later steps in the process [30]. Obtained results also revealed that phenolic acid extracts from the studied plants negatively affected the development of peach-potato aphid and bird cherry-oat aphid. Their influence was demonstrated by prolongation of the prereproductive period, a reduction in daily fecundity and a decrease in the intrinsic rate of natural increase. The results of our previous study [12] have shown that phenolic acids fraction obtained from Ribes nigrum L., Prunus cerasus L., and J. regia limited development of grain aphid on winter wheat. Reports of other authors also confirm bioactivity of plant extracts containing phenolic compounds. Wiesner et al. [31] observed significant reduction in the number of mustard aphid (Lipaphis erysimi Kalt.) on Brassica juncea L. after application plant extracts rich in phenolic acids. Moreover, Tomczyk and Suszko [32] demonstrated that negative effect of Salvia officinalis L. extract on mortality and fecundity spider mite (Tetranychus urticae Koch) was strictly connected with a high concentration of phenolic compounds in the tested mixture. Plant phenolics are well-known as allelochemicals that are highly toxic to aphids. They negatively influence the aphid feeding behavior, inhibit activity of numerous enzymes, reduce food uptake, and as a consequence prolong growth and development at both individual and population scale [33]. Earlier research by Leszczynski et al. [34] showed that application of phenolic acids can affect feeding and development of the bird cherry-oat aphid. Caffeic, ferulic and chlorogenic acids at a concentration of 62.5 mg L -1 inhibited the feeding of R. padi on winter wheat. Such phenolic acids as tannic acid and chlorogenic acid were also detrimental to S. graminum growth. Almost none of the progeny survived when these compounds were included in the artificial diet and the number of progeny was drastically reduced. The aphidicidal properties of tested phenolic acid extracts significantly varied, depending to the plant species and generally increased with higher extract concentration. The highest efficacy was observed after application phenolics from J. regia, 5718

6 followed by extracts from M. piperita, S. nigra and H. perforatum. Their action on M. persicae and R padi aphids can be attributed to the active metabolites obtained from these donor plants and suggest synergistic effect of all phenolic acids present in the tested mixtures. The phenomenon of additive impact is often crucial to bioactivity of plant-derived products. Rattan [35] described that a mixture of secondary metabolites may be a deterrent to insects for a longer period than single compounds. Furthermore, substantial amounts of individual phenolic compounds in mixtures could increase insect susceptibility more than single compound at higher concentration. According to Wang et al. [10], the applied concentrations towards insects could be lowered, if only active compounds are used. Extractions of plant material with appropriate solvents very often concentrate the allelochemicals and make their potency readily detectable by pests [36]. A comparison of the aphidicidal activity of extracts revealed that bird cherry-oat aphid was more sensitive to applied phenolic acid mixtures than peach-potato aphid. The differences in response between the studied pests may be a result of their different adaptations to herbivory. Specialists generally show a greater sensitivity and react at a lower concentrations than generalists, whereas generalists base their decision making on a much larger number of plant characteristics than the specialists [37]. The peach-potato aphid, as a typical generalist, is able to ingest a variety of plant food, and it is therefore expected to exhibit greater tolerance or even resistance toward plant allelochemicals. This trait, however, would not be expected for grass specialist such as R. padi, which is adapted to withstand secondary metabolites from lower number of plants. Moreover, polyphagous insects possess an efficient detoxication mechanisms that participate in neutralization of different group of xenobiotics [38]. Such adaptations to polyphagy may explain relatively low efficacy of the phenolic acid extracts towards M. persicae. We have concluded that phenolic acids mixtures extracted from J. regia, M. piperita, S. nigra and H. perforatum showed an insecticidal activity against the peach-potato aphid and bird cherry-oat aphid. Among the plant extracts, the most active were phenolic acids obtained from J. regia and M. piperita. Both extracts not only significantly reduced the number of aphids on plants, but also limited initial infestation in choice tests. However, further studies are required to determine whether the treatment with phenolic acid extracts provide similar results on field populations of the aphids. ACKNOWLEDGEMENTS This study was carried out with the financial support of the Siedlce University of Natural Science and Humanities (Scientific Research Project no. 245/08/S). REFERENCES [1] Guerrieri, E. and Digilio, M.C. (2008) Aphidplant interactions: a review. Journal of Plant Interactions, 3, [2] Hesler, L.S., Hadi, B. A.R. and Tharp, C.I. (2010) Bird cherry-oat aphid (Hemiptera: Sternorrhyncha, Aphidinae): Biology, pest status, and management in wheat. Trends in Entomology, 6, [3] Blackman, R.L. and Eastop, V.F. (2000) Aphids on the world s crops, An identification and information guide, 2nd ed.; John Willey & Sons, Chichester. [4] Boulogne, I., Petit, P., Ozier-Lafontaine, H., Desfontaines, L. and Loranger-Merciris, G. (2012) Insecticidal and antifungal chemicals produced by plants: a review. Environmental Chemistry Letters 10, [5] Isman, M.B. (2006) The role of botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annual Review of Entomology, 51, [6] Sayeda, F.F., Torkey, H.M. and Hala, A.Y. (2009) Natural extracts and their chemical constituents in relation to toxicity against whitefly (Bemisia tabaci) and aphid (Aphis craccivora). Australian Journal of Basic Applied Sciences, 3 (4), [7] Pavela, R. (2009) Effectiveness of some botanical insecticides against Spodoptera littoralis Boisduval (Lepidoptera: Noctudiae), Myzus persicae Sulzer (Hemiptera: Aphididae) and Tetranychus uriticae Koch (Acari: Tetranychidae). Plant Protection Science, 45(4), [8] Dang, Q.L., Lee, G.Y., Choi, Y.H., Choi G.J., Jang K.S., Park, M.S., Soh, H.S., Han Y.H., Lim, C.H. and Kim, J.C. (2010) Insecticidal activities of crude extracts and phospholipids from Chenopodium ficifolium against melon and cotton aphid, Aphis gossypii. Crop Protection, 29, [9] Zhai, Z.M., Zhang, F.Y., Wei, H.H. and Wang, W. (2006) A study on the bioactivity of secondary metabolites from walnut green hull. Journal of Northwest Forestry University 21, [10] Wang, Y., Shi, L., Zhao, L., Liu, S., Yu, T., Clarke, S. and Sun, J. (2007) Acaricidal activity of Juglans regia leaf extracts on Tetranychus 5719

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